Cortical Responses to the 2F1-F2 Combination Tone Measured Indirectly Using Magnetoencephalography
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Cortical responses to the 2f1-f2 combination tone measured indirectly using magnetoencephalography ͒ ͒ David W. Purcell,a Bernhard Ross ͑ß͒, Terence W. Picton, and Christo Pantevb Rotman Research Institute at Baycrest, 3560 Bathurst Street, Toronto, Ontario, M6A 2E1, Canada ͑Received 1 March 2007; revised 26 May 2007; accepted 29 May 2007͒ The simultaneous presentation of two tones with frequencies f1 and f2 causes the perception of several combination tones in addition to the original tones. The most prominent of these are at frequencies f2-f1 and 2f1-f2. This study measured human physiological responses to the 2f1-f2 combination tone at 500 Hz caused by tones of 750 and 1000 Hz with intensities of 65 and 55 dB SPL, respectively. Responses were measured from the cochlea using the distortion product otoacoustic emission ͑DPOAE͒, and from the auditory cortex using the 40-Hz steady-state magnetoencephalographic ͑MEG͒ response. The perceptual response was assessed by having the participant adjust a probe tone to cause maximal beating ͑“best-beats”͒ with the perceived combination tone. The cortical response to the combination tone was evaluated in two ways: first by presenting a probe tone with a frequency of 460 Hz at the perceptual best-beats level, resulting in a 40-Hz response because of interaction with the combination tone at 500 Hz, and second by simultaneously presenting two f1 and f2 pairs that caused combination tones that would themselves ͑ ͒ beat at 40 Hz. The 2f1-f2 DPOAE in the external auditory canal had a level of 2.6 s.d. 12.1 dB SPL. The 40-Hz MEG response in the contralateral cortex had a magnitude of 0.39 ͑s.d. 0.1͒ nA m. The perceived level of the combination tone was 44.8 ͑s.d. 11.3͒ dB SPL. There were no significant correlations between these measurements. These results indicate that physiological responses to the 2f1-f2 combination tone occur in the human auditory system all the way from the cochlea to the primary auditory cortex. The perceived magnitude of the combination tone is not determined by the measured physiological response at either the cochlea or the cortex. © 2007 Acoustical Society of America. ͓DOI: 10.1121/1.2751250͔ PACS number͑s͒: 43.64.Ri, 43.64.Jb, 43.64.Qh, 43.66.Ki ͓BLM͔ Pages: 992–1003 ͒ I. INTRODUCTION Goldstein, 1966; Smoorenburg, 1972a, b . The 2f1-f2 nonlin- earity is termed “essential” because it occurs at low stimulus The mammalian cochlea contains nonlinearities that levels ͑Goldstein, 1966͒. This is unlike a mainly linear sys- generate frequencies not present in the stimulus. The sim- tem distorting only at higher levels ͑von Helmholtz, 1877/ ͒ plest acoustic stimulus that can be used to study this phe- 1954; Goldstein, 1966 . The level and phase of the 2f1-f2 nomena is composed of two pure tones with frequencies f1 tone within the cochlea can be estimated by presenting an Ͼ and f2, where f2 f1. In response, the cochlea produces a set additional “cancellation” tone of the same frequency of combination tones, or distortion products, of which the ͑Zwicker, 1955; Goldstein, 1966, 1969͒. Perception of the cubic 2f1-f2 and the quadratic f2-f1 are the most prominent combination tone can be eliminated by carefully adjusting and most studied. the magnitude and phase of the cancellation tone until noth- With favorable stimulus conditions, combination tones ing is heard. Goldstein ͑1966͒ facilitated the subject’s ability are audible. The Italian violinist Tartini knew of their exis- to hear the cancellation effect by adding an additional probe tence as early as 1714 ͑Jones, 1935͒. As Jones ͑1935͒ re- tone slightly mistuned from the cancellation tone ͑e.g., ports, by 1801 it was known that the tone produced by a 4Hz͒, of sufficient level to beat with the combination tone. 32-ft pipe in a cathedral organ ͑about 16 Hz͒ could be gen- The cancellation tone was then adjusted to eliminate the erated in the ears of listeners by simultaneously activating a beating sensation by canceling the combination tone. Using 16-ft pipe ͑about 32 Hz͒ and an even shorter pipe producing the cancellation technique, the cochlear 2f1-f2 combination ͑ ͒ its fifth about 48 Hz through the 2f1-f2 combination tone, tone has an apparent level of an externally supplied tone that thus dispensing with the need for 32-ft pipes. is 20–40 dB below that of equal level primaries in the ex- ͑ The 2f1-f2 combination tone has been extensively stud- ternal ear canal where tone pair stimuli f2 and f1 have equal ied psychoacoustically ͑e.g., Zwicker, 1955; Plomp, 1965; levels L2 =L1; Goldstein, 1966; Smoorenburg, 1972b; Hall, 1975͒. Cancellation methods may overestimate the level of the combination tone for small f2 / f1 due to suppression ef- a͒ ͑ Author to whom correspondence should be addressed; Electronic mail: fects of the stimulus f1 Smoorenburg, 1972b; Shannon and [email protected]. Currently affiliated with the National Centre for Au- Houtgast, 1980; Zwicker, 1981͒. diology at the University of Western Ontario, London, Ontario, N6G 1H1, The psychoacoustically estimated levels of the combina- Canada. b͒ ͑ Currently affiliated with the Institute for Biomagnetism and Biosig- tion tones with respect to the stimuli i.e., 20–40 dB below nalanalysis at the University of Münster, Münster, Germany. the primaries͒ are similar to the levels of distortion products 992 J. Acoust. Soc. Am. 122 ͑2͒, August 20070001-4966/2007/122͑2͒/992/12/$23.00 © 2007 Acoustical Society of America measured in the mechanical motion of the basilar membrane is impossible to use time-domain measures such as the ͑Robles et al., 1997͒, the cochlear microphonic ͑Gibian and evoked N1 or sustained response. In contrast, steady-state Kim, 1982͒, receptor potentials of IHCs ͑Nuttall and Dolan, frequency-domain measurements of auditory evoked poten- 1990͒, and single fibers of the auditory nerve ͑Goldstein and tials and magnetic fields can separate the responses to the Kiang, 1968; Buunen and Rhode, 1978; Kim et al., 1980͒. stimuli and to the combination tones because they are at The response can be eliminated from recordings of nerve different frequencies. Unfortunately, steady-state responses fibers using cancellation techniques ͑Goldstein and Kiang, above 100 Hz derive mainly from brainstem sources ͑Herd- 1968; Goldstein et al., 1978͒. These results indicated that the man et al., 2002; Purcell et al., 2004͒, and combination tones 2f1-f2 combination tone is present in the cochlea, and sug- are most relevant at frequencies higher than 100 Hz. Steady- gested that it was processed at the same characteristic place state measurements cannot therefore directly measure the re- as an externally supplied tone of equal frequency. The 2f1-f2 sponse to the 2f1-f2 combination tone in cortex. To over- combination tone was later observed directly in the mechani- come these constraints, an approach based on beating used in cal motion of the basilar membrane at its characteristic place psychoacoustics was adopted ͑Goldstein, 1966; Furst et al., ͑Robles et al., 1991, 1997͒. 1988, unpublished͒.. Two pure tones that are similar in fre- The distortion product otoacoustic emission ͑DPOAE͒ at quency and magnitude will cause beating at the difference frequency 2f1-f2 is initially generated at the f2 characteristic frequency. Therefore, cortical correlates of the 2f1-f2 combi- place where the two stimulus tones interact most promi- nation tone could be measured indirectly by causing a 40-Hz nently ͑Talmadge et al., 1999; Shera and Guinan, 1999; beat either between a combination tone and an externally Knight and Kemp, 2000͒. Signals at the DPOAE frequency presented probe tone, or between two combination tones. then propagate on the basilar membrane both basally and The sensation of beating between a 2f1-f2 combination tone apically. The apical propagation will reach the characteristic and an externally supplied tone can be perceived relatively place for frequencies equal to 2f1-f2. The DPOAE measured easily by naïve participants with little training. The 40-Hz in the ear canal can be dominated by energy from either the steady-state magnetic fields generated in the auditory corti- ͑ f2 or the 2f1-f2 place depending on the stimulus parameters ces Mäkelä and Hari, 1987; Pantev et al., 1996; Gutschalk ͑Shera and Guinan, 1999; Knight and Kemp, 2000, 2001; et al., 1999; Schoonhoven et al., 2003͒ by these beats can be Dhar et al., 2005͒. Wilson ͑1980͒ found significant discrep- measured using MEG. ancies between the levels of the ear canal DPOAEs and psy- This indirect method of obtaining correlates of the choacoustic cancellation levels in the same subjects. These 2f1-f2 combination tone measures physiological responses to may have been in part due to changes in dominant DPOAE the difference-frequency type combination tone or “beat.” sources across stimulus conditions. However, Furst et al. Cochlear microphonic ͑Gibian and Kim, 1982; Cheatham ͑1988͒ and Zwicker and Harris ͑1990͒ also reported that and Dallos, 1997͒, IHC ͑Cheatham and Dallos, 1997͒, and DPOAE levels in the canal were low compared to those es- single neuron studies ͑Smoorenburg et al., 1976; Kim et al., timated psychoacoustically in the same subjects. Further- 1980͒ have shown that both cubic and quadratic combination more, the finding that psychoacoustic cancellation does not tones travel as waves on the basilar membrane from their eliminate the ear canal DPOAE highlights the fact that dif- initiation place where the stimuli interact at their own char- ferent processes are involved in the generation of the acteristic places. They are also present in nerve fiber record- DPOAE and the perception of the combination tone ͑Furst et ings both near the stimulus interaction site and at their own al., 1988; Zwicker and Harris, 1990͒.